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IMPORTANCE: The hyperarid Namib Desert is one of the oldest deserts on Earth. It contains multiple clusters of playas which are saline-rich springs surrounded by halite evaporites. Playas are of great ecological importance, and their indigenous (poly)extremophilic microorganisms are potentially involved in the precipitation of minerals such as carbonates and sulfates and have been of great biotechnological importance. While there has been a considerable amount of microbial ecology research performed on various Namib Desert edaphic microbiomes, little is known about the microbial communities inhabiting its multiple playas. In this work, we provide a comprehensive taxonomic and functional potential characterization of the microbial, including viral, communities of sediment mats and halites from two distant salt pans of the Namib Desert, contributing toward a better understanding of the ecology of this biome.
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Bactérias , Microbiota , Bactérias/genética , Clima Desértico , Microbiologia do Solo , Cloreto de SódioRESUMO
In a recent study, we found a distinct soil bacterial community associated with male and female plants of the desert gymnosperm Welwitschia mirabilis. In this subsequent study, we also found that the soil fungal community associated with Welwitschia differs between male and female plants, and between unvegetated areas and the soil under plants. Site location, pH, and soil moisture also had an important influence on the composition of the fungal community. A number of Ascomycota and Chytrid species were found to be distinct indicators of male and female plants, respectively, but there was no overall difference at the phylum level or in terms of diversity. The unvegetated areas between plants also differed in terms of several Ascomycota OTUs. Network connectivity of the fungal communities was found to be higher under both male and female Welwitschia plants than in unvegetated control areas. As with the bacterial community, it is unclear what processes produce the gender-distinct fungal community, and also the more general plant-associated community, and also what the effects on the biology of the plants are. One possibility behind the gender-related difference in fungal community is that there are differences in the production of pollen or nectar between the two plant genders, affecting the below-ground soil community.
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Ascomicetos , Mirabilis , Micobioma , Cycadopsida , Solo/química , Plantas/microbiologia , Microbiologia do SoloRESUMO
The ventral surfaces of translucent rocks from hot desert pavements often harbor hypolithic microbial communities, which are mostly dominated by cyanobacteria. The Namib Desert fog belt supports extensive hypolithic colonization of quartz rocks, which are also colonized by lichens on their dorsal surfaces. Here, we aim to evaluate whether lichens colonize the ventral surface of the rocks (i.e., show hypolithic lifestyle) and compare the bacterial composition of these coastal hypolithic communities with those found inland. Fungal DNA barcoding and fungal and bacterial Illumina metabarcoding were combined with electron microscopy to characterize the composition and spatial structure of hypolithic communities from two (coastal and inland) areas in the Namib Desert. We report, for the first time, the structure and composition of lichen-dominated hypolithic communities found in the coastal zone of the Namib Desert with extensive epilithic lichen cover. Lichen modified areoles with inverted morphology of the genus Stellarangia (three lineages) and Buellia (two lineages) were the main components of these hypolithic communities. Some of these lineages were also found in epilithic habitats. These lichen-dominated hypolithic communities differed in structural organization and bacterial community composition from those found in inland areas. The hypolithic lichen colonization characterized here seems not to be an extension of epilithic or biological soil crust lichen growths but the result of specific sublithic microenvironmental conditions. Moisture derived from fog and dew could be the main driver of this unique colonization.
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Cianobactérias , Líquens , Cianobactérias/genética , Clima Desértico , Ecossistema , Microbiologia do SoloRESUMO
In hyper-arid soil environments, photosynthetic microorganisms are largely restricted to hypolithic (sub-lithic) habitats: i.e., on the ventral surfaces of translucent pebbles in desert pavements. Here, we combined fluorometric, spectroscopic, biochemical and metagenomic approaches to investigate in situ the light transmission properties of quartz stones in the Namib Desert, and assess the photosynthetic activity of the underlying hypolithic cyanobacterial biofilms. Quartz pebbles greatly reduced the total photon flux to the ventral surface biofilms and filtered out primarily the short wavelength portion of the solar spectrum. Chlorophylls d and f were not detected in biofilm pigment extracts; however, hypolithic cyanobacterial communities showed some evidence of adaptation to sub-lithic conditions, including the prevalence of genes encoding Helical Carotenoid Proteins, which are associated with desiccation stress. Under water-saturated conditions, hypolithic communities showed no evidence of light stress, even when the quartz stones were exposed to full midday sunlight. This initial study creates a foundation for future in-situ and laboratory exploration of various adaptation mechanisms employed by photosynthetic organisms forming hypolithic microbial communities.
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Cianobactérias , Clima Desértico , Cianobactérias/genética , Ecossistema , Fotossíntese , Microbiologia do SoloRESUMO
Current Pennisetum glaucum (L.) R. BR. cultivars in Namibia have overall poor performance posing a threat to the nation's food security because this crop is staple for over 70% of the Namibian population. The crop suffers from undesirable production traits such as susceptibility to diseases, low yield, and prolonged reproductive cycle. This study aimed to understand the genetic diversity of the crop in Namibia by simple sequence repeats (SSRs) and morphology analysis. A total of 1441 genotypes were collected from the National Gene Bank representing all the Namibian landraces. A sample of 96 genotypes was further analyzed by SSR using Shannon-Wiener diversity index and revealed a value of 0.45 indicating low genetic diversity. Ordination using Principal Coordinate Analysis (PCoA) on SSR data confirmed clusters generated by UPGMA for the 96 P. glaucum accessions. UPGMA phenograms of 29 morphological characterized genotypes were generated for SSR and morphology data and the two trees revealed 78% resemblance. Lodging susceptibility, tillering attitude, spike density, fodder yield potential, early vigour, and spike shape were the phenotypic characters upon which some clusters were based in both datasets. It is recommended that efforts should be made to widen the current gene pool in Namibia.
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Variação Genética , Repetições de Microssatélites , Pennisetum/genética , Marcadores Genéticos , Genótipo , Namíbia , FenótipoRESUMO
Type I hypolithons are microbial communities dominated by Cyanobacteria. They adhere to the underside of semi-translucent rocks in desert pavements, providing them with a refuge from the harsh abiotic stresses found on the desert soil surface. Despite their crucial role in soil nutrient cycling, our understanding of their growth rates and community development pathways remains limited. This study aimed to quantify the dynamics of hypolithon formation in the pavements of the Namib Desert. We established replicate arrays of sterile rock tiles with varying light transmission in two areas of the Namib Desert, each with different annual precipitation regimes. These were sampled annually over 7 years, and the samples were analysed using eDNA extraction and 16S rRNA gene amplicon sequencing. Our findings revealed that in the zone with higher precipitation, hypolithon formation became evident in semi-translucent rocks 3 years after the arrays were set up. This coincided with a Cyanobacterial 'bloom' in the adherent microbial community in the third year. In contrast, no visible hypolithon formation was observed at the array set up in the hyper-arid zone. This study provides the first quantitative evidence of the kinetics of hypolithon development in hot desert environments, suggesting that development rates are strongly influenced by precipitation regimes.
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Cianobactérias , Clima Desértico , Microbiota , RNA Ribossômico 16S , Microbiologia do Solo , Cianobactérias/genética , Cianobactérias/isolamento & purificação , Cianobactérias/crescimento & desenvolvimento , Cianobactérias/classificação , Cianobactérias/metabolismo , RNA Ribossômico 16S/genética , Namíbia , Cinética , Filogenia , DNA Bacteriano/genética , Solo/químicaRESUMO
Rainfall is rare in hyperarid deserts but, when it occurs, it triggers large biological responses essential for the long-term maintenance of the ecosystem. In drylands, microbes play major roles in nutrient cycling, but their responses to short-lived opportunity windows are poorly understood. Due to its ephemeral nature, mRNA is ideally suited to study microbiome dynamics upon abrupt changes in the environment. We analyzed microbial community transcriptomes after simulated rainfall in a Namib Desert soil over 7 days. Using total mRNA from dry and watered plots we infer short-term functional responses in the microbiome. A rapid two-phase cycle of activation and return to basal state was completed in a short period. Motility systems activated immediately, whereas competition-toxicity increased in parallel to predator taxa and the drying of soils. Carbon fixation systems were downregulated, and reactivated upon return to a near-dry state. The chaperone HSP20 was markedly regulated by watering across all major bacteria, suggesting a particularly important role in adaptation to desiccated ecosystems. We show that transcriptomes provide consistent and high resolution information on microbiome processes in a low-biomass environment, revealing shared patterns across taxa. We propose a structured dispersal-predation dynamic as a central driver of desert microbial responses to rainfall.
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Ecossistema , Microbiota , Solo , Clima Desértico , Microbiologia do Solo , Microbiota/genética , Água , RNA MensageiroRESUMO
The Namib Desert is a hyperarid coastal desert where fog is a major moisture source. We hypothesized that the fog-harvesting grass Stipagrostis sabulicola establishes an important ecological niche, termed the "Fog-Plant-Oases" (FPOs), and serves as the primary carbon source for the invertebrate community. To determine this, we measured the natural variations of the stable carbon and nitrogen isotopes (δ13C and δ15N) of invertebrates as well as that of plant biomass and belowground detritus and estimated the contributions of the fog plants in their diets. Our findings revealed a complex trophic structure and demonstrated that S. sabulicola fuels carbon flow from lower to higher trophic levels in the aboveground food web. The distinct δ13C values of bacterial- and fungal-feeding nematodes indicated however the separation of the aboveground niche, which is primarily sustained by S. sabulicola, from the belowground niche, where wind-blown sediments may serve as the main energy source for the soil biota. Our findings further accentuate the critical role of S. sabulicola FPOs in establishing complex trophic dynamics and a distinctive food web within the hyperarid Namib dunes.
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Ecossistema , Cadeia Alimentar , Animais , Namíbia , Poaceae/metabolismo , Isótopos de Nitrogênio/análise , Isótopos de Nitrogênio/metabolismo , Isótopos de Carbono/análise , Biomassa , Clima Desértico , Solo/química , Carbono/metabolismo , InvertebradosRESUMO
Water availability is the dominant driver of microbial community structure and function in desert soils. However, these habitats typically only receive very infrequent large-scale water inputs (e.g., from precipitation and/or run-off). In light of recent studies, the paradigm that desert soil microorganisms are largely dormant under xeric conditions is questionable. Gene expression profiling of microbial communities in desert soils suggests that many microbial taxa retain some metabolic functionality, even under severely xeric conditions. It, therefore, follows that other, less obvious sources of water may sustain the microbial cellular and community functionality in desert soil niches. Such sources include a range of precipitation and condensation processes, including rainfall, snow, dew, fog, and nocturnal distillation, all of which may vary quantitatively depending on the location and geomorphological characteristics of the desert ecosystem. Other more obscure sources of bioavailable water may include groundwater-derived water vapour, hydrated minerals, and metabolic hydro-genesis. Here, we explore the possible sources of bioavailable water in the context of microbial survival and function in xeric desert soils. With global climate change projected to have profound effects on both hot and cold deserts, we also explore the potential impacts of climate-induced changes in water availability on soil microbiomes in these extreme environments.
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Soil nematodes are fundamentally aquatic animals, requiring water to move, feed, and reproduce. Nonetheless, they are ubiquitous in desert soils because they can enter an anhydrobiotic state that allows them to persist when water is biologically unavailable. In the hyper-arid Namib Desert of Namibia, rain is rare, but fog routinely moves inland from the coast and supports plant and animal life. Very little is understood about how this fog may affect soil organisms. We investigated the role of fog moisture in the ecology of free-living, soil nematodes across an 87-km fog gradient in the gravel plains of the Namib Desert. We found that nematodes emerged from anhydrobiosis and became active during a fog event, suggesting that they can utilize fog moisture to survive. Nematode abundance did not differ significantly across the fog gradient and was similar under shrubs and in interplant spaces. Interplant soils harbor biological soil crusts that may sustain nematode communities. As fog declined along the gradient, nematode diversity increased in interplant soils. In areas where fog is rare, sporadic rainfall events can stimulate the germination and growth of desert ephemerals that may have a lasting effect on nematode diversity. In a 30-day incubation experiment, nematode abundance increased when soils were amended with water and organic matter. However, these responses were not evident in field samples, which show no correlations among nematode abundance, location in the fog gradient, and soil organic matter content. Soil nematodes are found throughout the Namib Desert gravel plains under a variety of conditions. Although shown to be moisture- and organic matter-limited and able to use moisture from the fog for activity, variation in fog frequency and soil organic matter across this unique ecosystem may be biologically irrelevant to soil nematodes in situ.
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Plants have evolved unique morphological and developmental adaptations to cope with the abiotic stresses imposed by (hyper)arid environments. Such adaptations include the formation of rhizosheath-root system in which mutualistic plant-soil microbiome associations are established: the plant provides a nutrient-rich and shielded environment to microorganisms, which in return improve plant-fitness through plant growth promoting services. We hypothesized that the rhizosheath-root systems represent refuge niches and resource islands for the desert edaphic microbial communities. As a corollary, we posited that microorganisms compete intensively to colonize such "oasis" and only those beneficial microorganisms improving host fitness are preferentially selected by plant. Our results show that the belowground rhizosheath-root micro-environment is largely more hospitable than the surrounding gravel plain soil with higher nutrient and humidity contents, and cooler temperatures. By combining metabarcoding and shotgun metagenomics, we demonstrated that edaphic microbial biomass and community stability increased from the non-vegetated soils to the rhizosheath-root system. Concomitantly, non-vegetated soil communities favored autotrophy lifestyle while those associated with the plant niches were mainly heterotrophs and enriched in microbial plant growth promoting capacities. An intense inter-taxon microbial competition is involved in the colonization and homeostasis of the rhizosheath zone, as documented by significant enrichment of antibiotic resistance genes and CRISPR-Cas motifs. Altogether, our results demonstrate that rhizosheath-root systems are "edaphic mini-oases" and microbial diversity hotspots in hyperarid deserts. However, to colonize such refuge niches, the desert soil microorganisms compete intensively and are therefore prepared to outcompete potential rivals.
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The gymnosperm Welwitschia mirabilis belongs to the ancient, enigmatic gnetophyte lineage. It is a unique desert plant with extreme longevity and two ever-elongating leaves. We present a chromosome-level assembly of its genome (6.8 Gb/1 C) together with methylome and transcriptome data to explore its astonishing biology. We also present a refined, high-quality assembly of Gnetum montanum to enhance our understanding of gnetophyte genome evolution. The Welwitschia genome has been shaped by a lineage-specific ancient, whole genome duplication (~86 million years ago) and more recently (1-2 million years) by bursts of retrotransposon activity. High levels of cytosine methylation (particularly at CHH motifs) are associated with retrotransposons, whilst long-term deamination has resulted in an exceptionally GC-poor genome. Changes in copy number and/or expression of gene families and transcription factors (e.g. R2R3MYB, SAUR) controlling cell growth, differentiation and metabolism underpin the plant's longevity and tolerance to temperature, nutrient and water stress.
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Cycadopsida/genética , Clima Desértico , Genoma de Planta , África , Metilação de DNA/genética , Evolução Molecular , Geografia , Meristema/genética , Anotação de Sequência Molecular , Folhas de Planta/genética , Chuva , Análise de Sequência de DNA , Especificidade da Espécie , Transcriptoma/genéticaRESUMO
Desert and semi-desert plants are often associated with a distinct soil biota under the plants and close to the root system. We aimed to understand if similar effects could be found in the taxonomically isolated desert gymnosperm Welwitschia mirabilis in the Namib Desert, and whether this island effect varied with climate and with gender of plants. We took soil cores adjacent to the plants in environments ranging from extreme desert to arid shrubland, and in nearby control sites between the plants. Soil chemistry was analysed, and deoxyribonucleic acid was extracted and sequenced for the bacterial 16s region. Soil under the plants was richer in organic C, N and moisture. Despite the range of climates, the soil around Welwitschia plants was consistently associated with a particular bacterial community composition that was distinct from samples further away. Compared to unvegetated control patches, bacterial diversity close to the plants was reduced. In the plant-associated soil community, there was a clear gender effect across all sites with a distinct community composition and greater diversity under male plants. It is unclear what differences in the soil environment might be producing these gender-associated differences, which provide an additional dimension to the fertile island effect.
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Fármacos para a Fertilidade , Microbiota , Clima Desértico , Ecossistema , Ilhas , Masculino , Solo , Microbiologia do SoloRESUMO
Hot desert surface soils are characterized by extremely low water activities for large parts of any annual cycle. It is widely assumed that microbial processes in such soils are very limited. Here we present the first metatranscriptomic survey of microbial community function in a low water activity hyperarid desert soil. Sequencing of total mRNA revealed a diverse and active community, dominated by Actinobacteria. Metatranscriptomic analysis of samples taken at different times over 3 days indicated that functional diel variations were limited at the whole community level, and mostly affected the eukaryotic subpopulation which was induced during the cooler night hours. High levels of transcription of chemoautotrophic carbon fixation genes contrasted with limited expression of photosynthetic genes, indicating that chemoautotrophy is an important alternative to photosynthesis for carbon cycling in desiccated desert soils. Analysis of the transcriptional levels of key N-cycling genes provided strong evidence that soil nitrate was the dominant nitrogen input source. Transcriptional network analyses and taxon-resolved functional profiling suggested that nutrient acquisition processes, and not diurnal environmental variation, were the main drivers of community activity in hyperarid Namib Desert soil. While we also observed significant levels of expression of common stress response genes, these genes were not dominant hubs in the co-occurrence network.
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AIM: To assess spatial patterns of genetic and species-level diversity for Namib Desert Collembola using mitochondrial DNA cytochrome c oxidase subunit I (COI) gene sequences. LOCATION: Namib Desert gravel plains. TAXON: Collembola (springtails). METHODS: A total of 77 soil samples were collected along NE-SW (60 km) and E-W (160 km) transects from within a 4,000 km2 area of the Namib Desert gravel plains. We extracted 434 springtails from the 37 samples which contained Collembola and sequenced them at the COI gene locus. In the absence of specific taxonomic keys and previous genetic data for these taxa, we used Generalized Mixed Yule Coalescent (GMYC) analyses to provide putative species-level designations. RESULTS: We obtained 341 successful COI sequences, 175 of which were unique haplotypes. GMYC analyses identified 30 putative species, with up to 28% sequence divergence (uncorrected p-distance). The distribution of genetic variants was disjunct, with 97% of haplotypes and 70% of "GMYC species" found only at single sites. MAIN CONCLUSIONS: Dispersal events, although rare, may be facilitated by environmental events such as prevailing onshore winds or occasional flow of rainwater to the coast. We conclude that the high genetic diversity we observed is the result of ancient springtail lineages, patchy distribution of suitable habitats, and limited dispersal (gene flow) among habitable locations.
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Studies of microbial biogeography are often convoluted by extremely high diversity and differences in microenvironmental factors such as pH and nutrient availability. Desert endolithic (inside rock) communities are relatively simple ecosystems that can serve as a tractable model for investigating long-range biogeographic effects on microbial communities. We conducted a comprehensive survey of endolithic sandstones using high-throughput marker gene sequencing to characterize global patterns of diversity in endolithic microbial communities. We also tested a range of abiotic variables in order to investigate the factors that drive community assembly at various trophic levels. Macroclimate was found to be the primary driver of endolithic community composition, with the most striking difference witnessed between hot and polar deserts. This difference was largely attributable to the specialization of prokaryotic and eukaryotic primary producers to different climate conditions. On a regional scale, microclimate and properties of the rock substrate were found to influence community assembly, although to a lesser degree than global hot versus polar conditions. We found new evidence that the factors driving endolithic community assembly differ between trophic levels. While phototrophic taxa, mostly oxygenic photosynthesizers, were rigorously selected for among different sites, heterotrophic taxa were more cosmopolitan, suggesting that stochasticity plays a larger role in heterotroph assembly. This study is the first to uncover the global drivers of desert endolithic diversity using high-throughput sequencing. We demonstrate that phototrophs and heterotrophs in the endolithic community assemble under different stochastic and deterministic influences, emphasizing the need for studies of microorganisms in context of their functional niche in the community.
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BACKGROUND: The rhizosheath-root system is an adaptive trait of sandy-desert speargrasses in response to unfavourable moisture and nutritional conditions. Under the deserts' polyextreme conditions, plants interact with edaphic microorganisms that positively affect their fitness and resistance. However, the trophic simplicity and environmental harshness of desert ecosystems have previously been shown to strongly influence soil microbial community assembly. We hypothesize that sand-driven ecological filtering constrains the microbial recruitment processes in the speargrass rhizosheath-root niche, prevailing over the plant-induced selection. METHODS: Bacterial and fungal communities from the rhizosheath-root compartments (endosphere root tissues, rhizosheath and rhizosphere) of three Namib Desert speargrass species (Stipagrostis sabulicola, S. seelyae and Cladoraphis spinosa) along with bulk sand have been studied to test our hypothesis. To minimize the variability determined by edaphic and climatic factors, plants living in a single dune were studied. We assessed the role of plant species vs the sandy substrate on the recruitment and selection, phylogenetic diversity and co-occurrence microbial networks of the rhizosheath-root system microbial communities. RESULTS: Microorganisms associated with the speargrass rhizosheath-root system were recruited from the surrounding bulk sand population and were significantly enriched in the rhizosheath compartments (105 and 104 of bacterial 16S rRNA and fungal ITS copies per gram of sand to up to 108 and 107 copies per gram, respectively). Furthermore, each rhizosheath-root system compartment hosted a specific microbial community demonstrating strong niche-partitioning. The rhizosheath-root systems of the three speargrass species studied were dominated by desert-adapted Actinobacteria and Alphaproteobacteria (e.g. Lechevalieria, Streptomyces and Microvirga) as well as saprophytic Ascomycota fungi (e.g. Curvularia, Aspergillus and Thielavia). Our results clearly showed a random phylogenetic turnover of rhizosheath-root system associated microbial communities, independent of the plant species, where stochastic factors drive neutral assembly. Co-occurrence network analyses also indicated that the bacterial and fungal community members of the rhizosheath-root systems established a higher number of interactions than those in the barren bulk sand, suggesting that the former are more stable and functional than the latter. CONCLUSION: Our study demonstrates that the rhizosheath-root system microbial communities of desert dune speargrasses are stochastically assembled and host-independent. This finding supports the concept that the selection determined by the desert sand prevails over that imposed by the genotype of the different plant species.
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Bactérias/isolamento & purificação , Fungos/isolamento & purificação , Metagenômica/métodos , Poaceae/microbiologia , Actinobacteria/classificação , Actinobacteria/genética , Actinobacteria/isolamento & purificação , Alphaproteobacteria/classificação , Alphaproteobacteria/genética , Alphaproteobacteria/isolamento & purificação , Ascomicetos/classificação , Ascomicetos/genética , Ascomicetos/isolamento & purificação , Bactérias/classificação , DNA Bacteriano/genética , DNA Fúngico/genética , Clima Desértico , Fungos/classificação , Filogenia , Raízes de Plantas/microbiologia , Rizosfera , Análise de Sequência de DNA , Microbiologia do SoloRESUMO
The hyper-arid central region of the Namib Desert is characterized by quartz desert pavement terrain that is devoid of vascular plant covers. In this extreme habitat the only discernible surface covers are epilithic lichens that colonize exposed surfaces of quartz rocks. These lichens are highly susceptible to disturbance and so field surveys have been limited due to concerns about disturbing this unusual desert feature. Here we present findings that illustrate how non-destructive surveys based upon advanced photogrammetry techniques can yield meaningful and novel scientific data on these lichens. We combined 'structure from motion analysis,' computer vision and GIS to create 3-dimensional point clouds from two-dimensional imagery. The data were robust in its application to estimating absolute lichen cover. An orange Stellarangia spp. assemblage had coverage of 22.8% of available substrate, whilst for a black Xanthoparmelia spp. assemblage coverage was markedly lower at 0.6% of available substrate. Hyperspectral signatures for both lichens were distinct in the near-infra red range indicating that Xanthoparmelia spp. was likely under relatively more moisture stress than Stellarangia spp. at the time of sampling, and we postulate that albedo effects may have contributed to this in the black lichen. Further transformation of the data revealed a colonization preference for west-facing quartz surfaces and this coincides with prevailing winds for marine fog that is the major source of moisture in this system. Furthermore, a three-dimensional 'fly through' of the lichen habitat was created to illustrate how the application of computer vision in microbiology has further potential as a research and education tool. We discuss how advanced photogrammetry could be applied in astrobiology using autonomous rovers to add quantitative ecological data for visible surface colonization on the surface of Mars.